FARMERS’ ECONOMIC INTEREST IN DERMANYSSUS GALLINAE CONTROL

: Poultry red mite or Dermanyssus gallinae (De Geer, 1778) is the most significant poultry ectoparasite with regards to health and economy. It is a widely accepted opinion that D. gallinae can only be suppressed, with the current annual expenditure of 60 eurocents per layer. However, research indicates that D. gallinae can be controlled in other ways and eradicated from the production facilities and farms, and subsequent reinfestation can be prevented by implementing biosafety measures. This provides a long-term or permanent effect of D. gallinae control. From the aspect of economy, this means that after decades of increasing expenditures, farmers can first decrease, and then completely eliminate expenditures incurred by D. gallinae . Therefore, economic calculations should be based on an expert and comprehensive approach, which should itself be based on rational control, preventive veterinary medicine, i.e. D. gallinae control program. This would result in long-term savings. In 10 years’ time, 0.5 million euros would be saved per 100.000 layers. There are an estimated 4 billion infested layers worldwide .


Introduction
Poultry production is the field of animal husbandry which provides the largest portion of animal source foods for human consumption. Last decades have been marked by an intensive increase in egg production. Over the period from 1970 to 2007, the production of table eggs tripled and rose from 20 million to 60 million tons. According to FAO, the number of layers reached 4.93 billion in 2009 (FAO, 2010).
Poultry red mite is the most significant poultry ectoparasite with regards to health and economy (Nordenfors, 2000). Control of red poultry mites in the current situation, not paying enough attention to the choice of acaricidal products for control and methods, i.e. rational pharmacotherapy (suppression), professional application and the principle of preventive veterinary medicine. Therefore, simultaneously with the increase in egg production, the problem of prevalence and harmful effect of poultry red mite has also increased, together with the damage caused by inefficient, partly efficient, or illegal control (Giangaspero et al., 2011(Giangaspero et al., , 2017Marangi et al., 2012) Poultry red mite Poultry red mite, Dermanyssus gallinae (De Geer, 1778) is an invasive arthropod, successfully adapted to the conditions of modern poultry production (figure 1). Over 80% of commercial layer flocks, as well as parent and breeding flocks are affected by the invasion of this ectoparasite (Sparagano et al., 2009). Its small size (about 1 mm), mobility, ability to feed on a large number of species of birds and mammals, resistance to temperature conditions and starvation (Pavlićević et al., 2007b), extreme adaptability and development of resistance, large numbers and high reproductive potential, hidden way of life and night activity (Simić and Živković, 1958) are the traits of this parasite which enable its invasiveness. Poultry red mite is a problem of the flock, but also of the environment, thus jeopardising not just current, but also future flocks (Pavlićević et al., 2018b). In addition to biological traits of the parasites, the basis of this health and economic problem is a long-term wrong approach to D. gallinae control, which has been additionally exacerbated by the new changes (EU 1999/74/ЕC) in the technological conditions of housing layers (Pavlićević et al., 2016a(Pavlićević et al., , 2016c(Pavlićević et al., , 2019Flochlay et al., 2017).

Harmful effects
The harm caused by D. gallinae can be direct and indirect.Direct harm is caused by immediate parasitic action of D. gallinae: crawling on the body, stinging and bloodsucking. This results in poultry being afflicted by stress, anaemia due to blood loss, deteriorated general health state and immune status, aggravation and transmission of infectious diseases. Clinical manifestations in the flock are nervousness, pronounced health problems, increased mortality rates, reduced egg quality, and increased feed consumption (Emous 2005(Emous , 2017Flochlay et al., 2017). D. gallinae is a zoonosis and occupational disease (Cafiero et al., 2019). It also afflicts people, causing nervousness, itching, and changes on the skin. These problems can result in workers leaving their jobs or asking for compensation due to aggravated working conditions.
Further, indirect harm caused by D. gallinae occurs due to transmission and incorrect approach.
1. A young flock can be invaded in the rearing facility, and it can further transmit the infestation to a previously uninfested production facility, thus causing further damage. The disease caused by D. gallinae (Dermanyssosis) is a hidden flaw, but it can be detected if properly looked for. The condition necessary to avoid the damage is a correct forensic assessment and definition of legal relations (Pavlićević et al., 2003(Pavlićević et al., , 2018c. 2. Used cages and equipment are some of the key vectors of D. gallinae in intensive poultry production. When purchasing used cages and equipment, it is necessary to pay attention to possible invasion. Invaded cages and equipment should cost less, because they will incur unplanned sanitation expenditures for farmers (Pavlićević et al., 2016b(Pavlićević et al., , 2018c. 3. Transport cages for poultry transmit D. gallinae and thus cause damage (Pavlićević and Pavlović 2016b). 4. Incorrect work organisation on farms enables the transmission of invasion within the farm, from one house to another. 5. Incorrect choice of products and methods of control and/or their unprofessional application cannot provide efficient control of D. gallinae invasion, and it can cause damage. 6. Untimely D. gallinae control increases the damage by maximising direct harm, as well as making control more expensive, usually through higher consumption and lower efficacy of products. The production in highly infested flocks (++++) is not cost-effective. 7. Uncritical control is reflected in the application of illegal acaricides or inadequate application of registered products, which is harmful to human health, poultry and the environment. 8. The presence of D. gallinae on table eggs causes customers' disgust and aversion. 9. Highly infested flocks can result in abattoirs' refusal to accept the flock after the production period is finished.

Calculation
Expenditures incurred by the damage are added to the cost of products and implementation of control measures and they represent the farmers' total economic loss. In some cases, these expenditures can include the cost of preparation and sanitation of the consequences of application, such as the eggs which must be safely disposed of due to the withdrawal period (harmful chemical residue in eggs). Farmers' true economic loss is visible after one year, which is the duration of the production period, or over a longer period.
Farmers' economic loss is caused by the increased parasitic prevalence, intensity and extensity of the invasion, difficulty level of D. gallinae control, and cost of products and methods. Estimated cost per hen in the period from 2005 to 2017 increased by 40%, and it is 231 million euros annually for the whole of Europe. Annual expenditure caused by D. gallinae per hen is 60 euro cents, 15 of which are spent on the control and 45 on damage (1:3) (Emous, 2005(Emous, , 2017. Less successful, and especially unsuccessful control includes both types of expenditures. The less successful D. gallinae control measures are, the bigger total expenditure is for farmers. However, expenditures caused by D. gallinae and its control do not have to nor ought to occur simultaneously. Successful D. gallinae control implies only control expenditures for farmers, and, in time, even those are eliminated. For example, in 10 years' time, over 0.5 million euros would be saved per 100.000 layers (capacity of a medium size farm). If we apply the infestation rate to the number of layers (FАО, 2007), we get the figure of about 4 billion layers infested with D. gallinae worldwide. This is an approximate figure, since both the numbers of layers and infested flocks have risen in the meantime. For example, reports for Germany, the Netherlands, and Belgium put D. gallinae infestation in layer flocks at 94% (Mul et al., 2016).

Current control
Current D. gallinae control offers a large selection of products. In the purpose of clarity, we have selected just two most important groups of products.
Since the beginning of modern intensive poultry production, D. gallinae control has predominantly been based on acaricides, synthetic neurotoxic compounds. Its purpose is D. gallinae suppression and its effects last for several months, or in some cases for over six months (Pavlićević, 2005;Pavlićević et al., 2016Pavlićević et al., , 2018d.
Over the past 10 years, with the development of SiO2 formulations, a technology which can compete with acaricides has been developed for the first time. However, the progress achieved with SiO2 has not been properly utilised, but has also been employed just in the purpose of D. gallinae suppression.
No developmental steps taken so far indicate any future change in the widely accepted approach to D. gallinae control. The control program for D. gallinae has been developed in contrast to the predominant approach. However, for over 20 years, it has remained marginalised and without any significant impact on the mainstream red mite control in the poultry industry.

Program
The problem of D. gallinae control can be solved and it does not have to exist in the poultry industry. The solution is a program, a comprehensive approach which would be based on preventive veterinary medicine and rational pharmacotherapy (control). The primary goal of the program in intensive poultry production is to prevent D. gallinae infestation in uninfested poultry houses, i.e. farms. Safety risks need to be excluded in infested houses, rational control needs to be introduced, and then efficacy and cost-effectiveness will be increased. After the necessary conditions have been met, D. gallinae is eradicated from the production facilities on the farm, and biosafety measures are introduced (Pavlićević et al., 2018a(Pavlićević et al., , 2018b. For example, if a highly effective suppression of D. gallinae is achieved by two treatments (during housing preparation, before the population) with P 547/17 (project ID 1115), in the partial absence of adequate conditions, mites will appear in small numbers only in the final three months. A small mite infestation (from + to ++) has no significant (measurable) health impact and it does not cause economic loss. If there are adequate conditions (hygienic conditions and housing downtime), the procedure of housing preparation with P 547/17 technology results in D. gallinae eradication from production facilities. In this case, the flock is not exposed even to minimal D. gallinae presence, i.e. its harmful effect, and therefore these harmful consequences do not exist anymore. If there is continued implementation of biosafety measures, the expenditures caused by harmful effect or further control are excluded in the future.
During its development, the program has relied on the current, available products and methods. Initially, it was based on acaricides. However, contrary to the widely accepted method of control (which required more frequent use of acaricides), a correct acaricide application in the poultry house (eradication and introduction of biosafety measures) eliminates the need for further acaricide use (Pavlićević et al., 2016).
The first practically applicable distancing from acaricide control was enabled by SiO2-based formulations. By exploring the possibilities of mechanical control, an original program was developed, based on the combination of powdered and liquid forms. Eradication was possible again, this time based on a mechanical method. However, an expensive and complex technological procedure, highly demanding regarding the necessary conditions, hindered its wider implementation.
Main disadvantages of SiO2-based product application have been successfully overcome first by developing a specialised formulation based on inert oils (P 547/17, Pulcap), and then by developing an original technology of its application (Project ID 1115). The new formulation and technology has been tested in laboratory (Pavlićević et al., 2017a(Pavlićević et al., , 2017c and clinical conditions. In this way, we have eliminated any safety risks and devised a more functional and efficient and less complex application procedure which requires fewer conditions. There is no possibility for D. gallinae to develop resistance to P 547/17 or to significantly adapt its behaviour. Therefore, the current program will not lose its efficacy over time. Its results are permanent. In comparison to other programs and methods for poultry red mite control, we have concluded that P 547/17 formulation and application technology is an example of rational D. gallinae control (Pavlićević et al., 2017b(Pavlićević et al., , 2019b. Moreover, it provides all the conditions necessary to completely exclude the application of neurotoxic synthetic compounds from poultry meat and egg production. P 547/17 formulation and application technology has its requirements: professional application, hygienic conditions, housing downtime. Furthermore, despite its undisputed quality, it has certain disadvantages, thus leaving more space to further improve this type of control. This program is permanently open for all new contributions to D. gallinae control, which would help it to function better and more adequately respond to various practical challenges of modern poultry industry.
A systematic approach to the implementation of D. gallinae control would be an adequate step towards intensive vertical and horizontal integration of poultry industry. Systematic program implementation would additionally contribute to functional and rational product application, protection of human and animal health and environment, and improved control of diseases transmitted by D. gallinae; improving the flock's general health status and increasing production results would result in farmers' economic gain.
The situation for D. gallinae control in extensive poultry production is different from the one in the intensive production, and consequently, the approach of the program is different. In extensive poultry production, there is an open system, contact with other domestic and wild animals, large area per layer, and complex environment. It is advised to correctly build and set up the perches and nests, together with the barriers which successfully divide them from the rest of the environment. In this way, farmers can control D. gallinae problem easily and without significant expenses (P 2017/ 0762).
The necessary conditions have been met to first stop the unfavourable trend in D. gallinae control, then mitigate the problem, and eventually eliminate it completely. All this cannot be achieved immediately, since the procedure is technologically demanding and complex.

Veterinary medicine
Insufficient efficacy of veterinary medicine in D. gallinae control effected the size and extent of economic loss suffered by farmers. Veterinary medicine could have contributed more to the mitigation and prevention of loss caused by D. gallinae in the following ways: 1. The primary role of veterinary medicine should have been to provide timely and correct information to farmers. In this way, the disease could have been stopped in its initial phase, and most farms would have been protected by biosafety measures, while the rest would have been easily treated. Well-informed farmers would have taken an active role in the solution of the problem, otherwise they make wrong decisions and become a part of the problem (Pavlićević et al., 2016); 2. Defining eradication as the objective of the control in intensive poultry production is the premise for a real solution. The generally accepted opinion in veterinary medicine that D. gallinae can only be suppressed puts the farmers in a hopeless position of constant, increasing expenditures (Pavlićević et al., 2018(Pavlićević et al., , 2018b; 3. Improved detection and standardised laboratory and clinical testing of efficacy of products and methods for D. gallinae control (Pavlićević et al., 2007a(Pavlićević et al., , 2017b(Pavlićević et al., , 2019c; 4. Warning about technological flaws and negative effects of complex cages and equipment, which would contribute to the improvement of conditions for D. gallinae control (Pavlićević et al., 2016a); 5. Timely utilisation of the legislation change in the EU regarding cages and equipment (ЕU 1999/74/ЕC) could have easily eliminated the problem. However, the omission to do so had the opposite effect and actually contributed to the spread of the disease (Pavlićević and Pavlović 2016a); 6. Insisting on rational control, advising the farmers about the optimal choice of current products and methods, based on verified data; 7. Ensuring professional application of products and methods, which is crucial for efficient control; 8. Insisting on preventive veterinary medicine and maximising the efficacy of control relative to the cost; 9. Regular tests of resistance and timely elimination of unjustified use of acaricides which have already caused resistance (Pavlićević et al., 2016); 10. Promoting integrated health care, especially with regards to the control of infectious diseases transmitted by D. gallinae , which would additionally improve the general health status of poultry and contribute to the general welfare and cost-effectiveness of poultry production (Pavlićević et al., 2017b); 11. Improving the efficacy of D. gallinae control and residue monitoring and minimise or completely exclude the toxicological risk caused by uncritical control (Pavlićević et al., 2005(Pavlićević et al., , 2018c; 12. Introduction of the control program would cover all the above said requirements (Pavlićević et al., 2018a(Pavlićević et al., , 2018b(Pavlićević et al., , 2019d.
We are facing an open questionto what extent does veterinary medicine fulfil its role in D. gallinae control? Farmers' economic interest is currently not in accordance with the generally accepted opinion in veterinary medicine regarding D. gallinae control. The future will provide the answer to the question to what extent it is possible to critically review and improve the above-mentioned positions of veterinary medicine in accordance with the basic medical principles and in the interest of general welfare and economic interest of farmers.

Conclusion
The economic interest of poultry producers can be significantly improved. Farmers' expenditures incurred by D. gallinae can be reduced (time necessary to meet the conditions), and subsequently completely eliminated. Improving farmers' economic interest from the aspect of D. gallinae control is in correlation with the general welfare (interest). The requirements necessary in order to achieve the said interest depend on the role of veterinary medicine, which should reconsider the current procedure of D. gallinae control and introduce the principles of rational control and preventive veterinary medicine, i.e. the control program.